Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter April 13, 2018

Characterization of the complete mitochondrial genome of Metastrongylus salmi (M. salmi) derived from Tibetan pigs in Tibet, China

Kun Li, Muhammad Shahzad, Hui Zhang, Khalid Mehmood, Xiong Jiang, Houqiang Luo, Lihong Zhang, Xiaoqian Dong and Jiakui Li
From the journal Acta Parasitologica

Abstract

The present study was designed to determine and analyze the mt genomes of Metastrongylus salmi (M. salmi), and reveal the phylogenetic relationships of this parasite using mt DNA sequences. Results showed that the complete mt genome of M. salmi was 13722 bp containing 12 protein-coding genes (cox1-3, nad1-6, nad4L, atp6 and cytb), 22 transfer RNA genes, and 2 ribosomal RNA genes (rrnL and rrnS). The overall A+T content was 73.54% and the nucleotide composition was A (23.52%), C (6.14%), G (19.60%), T (50.02%), and N (UCAG) (0.73%). A total of 4237 amino acids are encoded from the Tibetan isolates of M. salmi mt genomes. The ATA was predicted as the most common starting codon with 41.7% (5/12 protein genes); and 11 of the 12 protein genes were found to have a TAG or TAA translation termination codon. By clustering together the phylogenetic trees of Tibetan M. salmi and Austrian M. salmi, the M. salmi isolated from Tibetan pigs was found to be highly homological with that stemmed from Austrian one. This information provides meaningful insights into the phylogenetic position of the M. salmi China isolate and represents a useful resource for selecting molecular markers for diagnosis and population studies.

Acknowledgments

The current research was supported by the Key Science Fund of Science and Technology Agency of Tibet Autonomous Region and projects in the National Science & Technology Pillar Program during the 12th Five-year Plan Period (2012BA D3B03). Kun Li is supported by China Scholarship Council under Grant No. 201706760018.

  1. Conflict of interest: The authors state that there are no competing interests.

  2. Ethics statement: All procedures were performed in accordance with the laws, regulations, and strict guidelines of the Laboratory Animals Research Centre of Hubei province, P. R. China. Samples were collected with the permission of the relevant institutions and by following the parameters as set by the ethics committee of Huazhong Agricultural University (Permit number: 4200695757).

References

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–41010.1016/S0022-2836(05)80360-2Search in Google Scholar PubMed

Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. 2000. Gene Ontology: tool for the unification of biology. Nature Genetics, 25, 25–2910.1038/75556Search in Google Scholar PubMed PubMed Central

Benson G. 1999 Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research, 27, 573–58010.1093/nar/27.2.573Search in Google Scholar PubMed PubMed Central

Borgstrom E., Lundin S., Lundeberg J. 2011. Large scale library generation for high throughput sequencing. PLoS One, 6, e19119. DOI: 10.1371/journal.pone.001911910.1371/journal.pone.0019119Search in Google Scholar PubMed PubMed Central

Chiaromonte F., Yap V.B., Miller W. 2002. Scoring pairwise genomic sequence alignments. Pacific Symposium on Biocomputing, 7, 115–12610.1142/9789812799623_0012Search in Google Scholar PubMed

Cronn R., Liston A., Parks M., Gernandt D.S., Shen R.K. 2008. Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucleic Acids Research, 36, e12210.1093/nar/gkn502Search in Google Scholar PubMed PubMed Central

Durent L., Mouchiroud D. 1999. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila and Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 96, 4482–448710.1073/pnas.96.8.4482Search in Google Scholar PubMed PubMed Central

García-González Á.M., Pérez-Martín J.E., Gamito-Santos J.A., Calero-Bernal R., Alonso M.A., Carrión E.M. 2013. Epidemiologic study of lung parasites (Metastrongylus spp.) in wild boar (Sus scrofa) in southwestern Spain. Journal of Wildlife Disease, 49, 157–162. 10.7589/2011-07-217Search in Google Scholar PubMed

Gassó D., Rossi L., Mentaberre G., Casas E., Velarde R., Nosal P., et al. 2014. An identification key for the five most common species of Metastrongylus. Parasitology Research, 113, 3495–3500. 10.1007/s00436-014-4001-ySearch in Google Scholar PubMed

Helfenbein K.G., Brown W.M., Boore J.L. 2001. The complete mitochondrial genome of the articulate brachiopod Terebratalia transversa. Molecular Biology and Evolution, 18, 1734–174410.1093/oxfordjournals.molbev.a003961Search in Google Scholar PubMed

Hu M., Chilton N.B., Gasser R.B. 2003. The mitochondrial genome of Strongyloides stercoralis (Nematoda)-idiosyncratic gene order and evolutionary implications. International Journal of Parasitology, 33, 1393–140810.1016/S0020-7519(03)00130-9Search in Google Scholar

Humbert J.F., Drouet J. 1990. Enquête épidémiologique sur la métastrongylose du sanglier (Sus scrofa) en France. Gibier Faune Sauvag, 7, 67–84. (In French)Search in Google Scholar

Jex A.R., Hall R.S., Littlewood D.T., Gasser R.B. 2010. An integrated pipeline for next-generation sequencing and annotation of mitochondrial genomes. Nucleic Acids Research, 38, 522–533 Kanehisa M. 1997. A database for post-genome analysis. Trends in Genetics, 13, 37510.1093/nar/gkp883Search in Google Scholar PubMed PubMed Central

Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K.F., Itoh M., Kawashima S., et al. 2006. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Research, 34, D354–D35710.1093/nar/gkj102Search in Google Scholar PubMed PubMed Central

Kanehisa M., Goto S., Kawashima S., Okuno Y., Hattori M. 2004. The KEGG resource for deciphering the genome. Nucleic Acids Research, 32, D277–D28010.1093/nar/gkh063Search in Google Scholar PubMed PubMed Central

Kurtz S., Phillippy A., Delcher A.L., Smoot M., Shumway M., Antonescu C., Salzberg S.L. 2004. Versatile and open software for comparing large genomes. Genome Biology, 5, R1210.1186/gb-2004-5-2-r12Search in Google Scholar PubMed PubMed Central

Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., et al. 2009. The Sequence Alignment/Map (SAM) format and SAMtools. Bioinformatics, 25, 2078–207910.1093/bioinformatics/btp352Search in Google Scholar PubMed PubMed Central

Li K., Lan Y.F., Luo H.Q., Shahzad M., Zhang H., Wang L., et al.2017a. Prevalence of three Oesophagostomum spp. from Ti-betan pigs analyzed by genetic markers of nad1, cox3 and ITS1. Acta Parasitologica, 62, 90–96. 10.1515/ap-2017-0010Search in Google Scholar PubMed

Li K., Luo H.Q., Zhang H., Lan Y.F., Han Z.Q., Shahzad M., et al.2016. First report of Metastrongylus pudendotectus by the genetic characterization of mitochondria genome of cox1 in pigs from Tibet, China. Veterinary Parasitology, 223, 91–95. 10.1016/j.vetpar.2016.04.036Search in Google Scholar PubMed

Li K., Zhang L.H., Zhang H., Lei Z.X., Luo H.Q., Mehmood K., et al.2017b. Epidemiology investigation and risk factors of Echinococcus granulosus in yaks (Bos grunniens), Tibetan pigs and Tibetans on the Qinghai Tibetan plateau. Acta Tropica 173, 147–152. 10.1016/j.actatropica.2017.06.019Search in Google Scholar PubMed

Li M.W., Lin R.Q., Song H.Q., Wu X.Y., Zhu X.Q. 2008. The complete mitochondrial genomes for three Toxocara species of human and animal health significance. BMC Genomics, 9, 22410.1186/1471-2164-9-224Search in Google Scholar PubMed PubMed Central

Li R., Zhu H., Ruan J., Qian W., Fang X., Shi Z., et al. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Research, 20, 265–27210.1101/gr.097261.109Search in Google Scholar PubMed PubMed Central

Li X.R. (Ed.) 2011. Color atlas of animal parasitosis (2nd Edition). Beijing: China Agriculture PressSearch in Google Scholar

Lin R.Q., Liu G.H., Hu M., Song H.Q., Wu X.Y., Li M.Y., et al.2012. Oesophagostomum dentatum and Oesophagostomum quadrispinulatum: characterization of the complete mitochondrial genome sequences of the two pig nodule worms. Experimental Parasitology 131, 1–7. 10.1016/j.exp-para.2012.02.015Search in Google Scholar PubMed

Lohse M., Drechsel O., Bock R. 2007. Organellar Genome DRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current Genetics, 52, 267–27410.1007/s00294-007-0161-ySearch in Google Scholar PubMed

Magrane M. 2011. UniProt. Knowledgebase: a hub of integrated protein data. Databases-Oxford, 2011, 9. 10.1093/data-base/bar009Search in Google Scholar

Marruchella G., Paoletti B., Speranza R., Di Guardo G. 2012. Fatal bronchopneumonia in a Metastrongylus elongatus and Porcine circovirus type 2 co-infected pig. Research in Veterinary Science, 93, 310–312. 10.1016/j.rvsc.2011.05.016Search in Google Scholar PubMed

Romero H., Zavala A., Musto H. 2000. Codon usage in Chlamydia trachomatis is the result of strand-specific mutational biases and a complex pattern of selective force. Nucleic Acids Research, 28, 2084–209010.1093/nar/28.10.2084Search in Google Scholar PubMed PubMed Central

Saha S., Bridges S., Magbanua Z.V., Peterson D.G. 2008. Empirical comparison of ab initio repeat finding programs. Nucleic Acids Research, 36, 2284–229410.1093/nar/gkn064Search in Google Scholar PubMed PubMed Central

Singer G.A., Hickey D.A. 2000. Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Molecular Biology and Evolution, 17, 1581–158810.1093/oxfordjournals.molbev.a026257Search in Google Scholar PubMed

Sorensen M., Sanz A., Gómez J., Pamplona R., Portero-Otín M., Gredilla R., Barja G. 2006. Effects of fasting on oxidative stress in rat liver mitochondria. Free Radical Research, 40, 339–34710.1080/10715760500250182Search in Google Scholar PubMed

Tannistha N., Catherine O., Arvind P.S., Boddey J., Atkins T., Sarkar-Tyson M., et al. 2010. A genomic survey of positive selection in Burkholderia pseudomallei provides insights into the evolution of accidental virulence. PLoS Pathogens, 6, 1–1510.1371/journal.ppat.1000845Search in Google Scholar PubMed PubMed Central

Tatusov R.L., Fedorova N.D., Jackson J.D., Jacobs A.R., Kiryutin B., Koonin E.V., et al. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics, 4, 4110.1186/1471-2105-4-41Search in Google Scholar PubMed PubMed Central

Tatusov R.L., Koonin E.V., Lipman D.J. 1997. A genomic perspective on protein families. Science, 278, 631–63710.1126/science.278.5338.631Search in Google Scholar PubMed

Wyman S.K., Jansen R.K., Boore J.L. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics, 20, 3252–325510.1093/bioinformatics/bth352Search in Google Scholar PubMed

Zhang N.Z., Zhou D.H., Huang S.Y., Wang M., Shi X.C., Ciren D.B., Zhu X.Q. 2014. Seroprevalence and risk factors associated with Haemophilus parasuis infection in Tibetan pigs in Tibet. Acta Tropica, 132, 94–97. 10.1016/j.actatropica.2013.12.021Search in Google Scholar PubMed

Zhao G.H., Hua B., Cheng W.Y., Jia Y.Q., Li H.M., Yu S.K., Liu G.H. 2013. The complete mitochondrial genomes of Oesophagostomum asperum and Oesophagostomum columbianum in small ruminants. Infection. Infection Genetics and Evolution, 19, 205–211. 10.1186/1756-3305-7-319Search in Google Scholar PubMed PubMed Central

Received: 2017-7-12
Revised: 2017-12-29
Accepted: 2018-1-18
Published Online: 2018-4-13
Published in Print: 2018-6-26

© 2018 W. Stefański Institute of Parasitology, PAS

Scroll Up Arrow